Functional Analysis of a Divergent System II Protein, Ccs1, Involved in c-Type Cytochrome Biogenesis

Dreyfuss, Beth Welty; Hamel, Patrice; Nakamoto, Stacie S.; Merchant, Sabeeha

doi:10.1074/jbc.m208652200

Cited by 46 publications

(46 citation statements)

References 90 publications

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“…The domain topology was demonstrated using lacZ and phoA methods. In C. reinhardtii, CcsB (Ccs1) appears to be present but at re- on May 10, 2018 by guest http://jb.asm.org/ duced levels in strains with a ccsA mutation or any of three other ccs mutations (14). In another study by Hamel and colleagues, CcsB appears to migrate in a complex on native gels, but this putative complex is not present in a ccsA mutant (21).…”

Section: And 5 [Example Of Results With Cb75])mentioning

confidence: 99%

Mutations in Cytochrome Assembly and Periplasmic Redox Pathways inBordetella pertussis

et al. 2005

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Transposon mutagenesis of Bordetella pertussis was used to discover mutations in the cytochrome c biogenesis pathway called system II. Using a tetramethyl-p-phenylenediamine cytochrome c oxidase screen, 27 oxidasenegative mutants were isolated and characterized. Nine mutants were still able to synthesize c-type cytochromes and possessed insertions in the genes for cytochrome c oxidase subunits (ctaC, -D, and -E), heme a biosynthesis (ctaB), assembly of cytochrome c oxidase (sco2), or ferrochelatase (hemZ). Eighteen mutants were unable to synthesize all c-type cytochromes. Seven of these had transposons in dipZ (dsbD), encoding the transmembrane thioreduction protein, and all seven mutants were corrected for cytochrome c assembly by exogenous dithiothreitol, which was consistent with the cytochrome c cysteinyl residues of the CXXCH motif requiring periplasmic reduction. The remaining 11 insertions were located in the ccsBA operon, suggesting that with the appropriate thiol-reducing environment, the CcsB and CcsA proteins comprise the entire system II biosynthetic pathway. Antiserum to CcsB was used to show that CcsB is absent in ccsA mutants, providing evidence for a stable CcsA-CcsB complex. No mutations were found in the genes necessary for disulfide bond formation (dsbA or dsbB). To examine whether the periplasmic disulfide bond pathway is required for cytochrome c biogenesis in B. pertussis, a targeted knockout was made in dsbB. The DsbB ؊ mutant makes holocytochromes c like the wild type does and secretes and assembles the active periplasmic alkaline phosphatase. A dipZ mutant is not corrected by a dsbB mutation. Alternative mechanisms to oxidize disulfides in B. pertussis are analyzed and discussed.

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Section: And 5 [Example Of Results With Cb75])mentioning

confidence: 99%

Mutations in Cytochrome Assembly and Periplasmic Redox Pathways inBordetella pertussis

et al. 2005

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“…The system II pathway emerged in the mid-1990s through genetic analyses of Chlamydomonas (47,80,159,160) and selected bacteria such as Bacillus (92,139,140) and Bordetella (23,55,86) (Fig. 2).…”

Section: System Ii: Ccsb and Ccsa Form A Heme Channel And Cytochrome mentioning

confidence: 99%

“…The CcsBA (H77A) protein contains fourfold less heme in its external heme binding domain. All four histidines in the recombinant CcsBA are required for synthesis of a cytochrome c (59), and they are also required in the Chlamydomonas CcsA (71) and CcsB (Ccs1) (47). Remarkably, the H77A and H858A TMD mutants are complemented for function by adding exogenous imidazole, but the histidine mutants that comprise the external heme binding domain are not (59).…”

Section: System Ii: Ccsb and Ccsa Form A Heme Channel And Cytochrome mentioning

confidence: 99%

CytochromecBiogenesis: Mechanisms for Covalent Modifications and Trafficking of Heme and for Heme-Iron Redox Control

Kranz¹,

Richard-Fogal²,

Taylor

et al. 2009

Microbiol Mol Biol Rev

230

372

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SUMMARY Heme is the prosthetic group for cytochromes, which are directly involved in oxidation/reduction reactions inside and outside the cell. Many cytochromes contain heme with covalent additions at one or both vinyl groups. These include farnesylation at one vinyl in hemes o and a and thioether linkages to each vinyl in cytochrome c (at CXXCH of the protein). Here we review the mechanisms for these covalent attachments, with emphasis on the three unique cytochrome c assembly pathways called systems I, II, and III. All proteins in system I (called Ccm proteins) and system II (Ccs proteins) are integral membrane proteins. Recent biochemical analyses suggest mechanisms for heme channeling to the outside, heme-iron redox control, and attachment to the CXXCH. For system II, the CcsB and CcsA proteins form a cytochrome c synthetase complex which specifically channels heme to an external heme binding domain; in this conserved tryptophan-rich “WWD domain” (in CcsA), the heme is maintained in the reduced state by two external histidines and then ligated to the CXXCH motif. In system I, a two-step process is described. Step 1 is the CcmABCD-mediated synthesis and release of oxidized holoCcmE (heme in the Fe+3 state). We describe how external histidines in CcmC are involved in heme attachment to CcmE, and the chemical mechanism to form oxidized holoCcmE is discussed. Step 2 includes the CcmFH-mediated reduction (to Fe+2) of holoCcmE and ligation of the heme to CXXCH. The evolutionary and ecological advantages for each system are discussed with respect to iron limitation and oxidizing environments.

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“…Antibodies against D1, PsaA, and Rubisco LS were purchased from Agrisera. Other antibodies were described previously: cytochrome b 6 f subunits (Kuras and Wollman, 1994), ATP synthase subunit b (Drapier et al, 1992), CCBs , CCS1 (Dreyfuss et al, 2003), CCS5 (Gabilly et al, 2010), PTOX2 (HouilleVernes et al, 2011), and NDA2 (Desplats et al, 2009). TCA1-Flag and MCA1-HA were detected by ECL using monoclonal antibodies against the tags anti-Flag M2 (Sigma-Aldrich), anti HA.11 (Covance), and horseradish peroxidase-conjugated antibody against mouse IgG (Promega).…”

Section: Protein Preparation Separation and Analysismentioning

confidence: 99%

Nitric Oxide–Triggered Remodeling of Chloroplast Bioenergetics and Thylakoid Proteins upon Nitrogen Starvation inChlamydomonas reinhardtii

et al. 2014

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Starving microalgae for nitrogen sources is commonly used as a biotechnological tool to boost storage of reduced carbon into starch granules or lipid droplets, but the accompanying changes in bioenergetics have been little studied so far. Here, we report that the selective depletion of Rubisco and cytochrome b 6 f complex that occurs when Chlamydomonas reinhardtii is starved for nitrogen in the presence of acetate and under normoxic conditions is accompanied by a marked increase in chlororespiratory enzymes, which converts the photosynthetic thylakoid membrane into an intracellular matrix for oxidative catabolism of reductants. Cytochrome b 6 f subunits and most proteins specifically involved in their biogenesis are selectively degraded, mainly by the FtsH and Clp chloroplast proteases. This regulated degradation pathway does not require light, active photosynthesis, or state transitions but is prevented when respiration is impaired or under phototrophic conditions. We provide genetic and pharmacological evidence that NO production from intracellular nitrite governs this degradation pathway: Addition of a NO scavenger and of two distinct NO producers decrease and increase, respectively, the rate of cytochrome b 6 f degradation; NO-sensitive fluorescence probes, visualized by confocal microscopy, demonstrate that nitrogen-starved cells produce NO only when the cytochrome b 6 f degradation pathway is activated.

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Functional Analysis of a Divergent System II Protein, Ccs1, Involved in c-Type Cytochrome Biogenesis

Cited by 46 publications

References 90 publications

Mutations in Cytochrome Assembly and Periplasmic Redox Pathways inBordetella pertussis

Mutations in Cytochrome Assembly and Periplasmic Redox Pathways inBordetella pertussis

CytochromecBiogenesis: Mechanisms for Covalent Modifications and Trafficking of Heme and for Heme-Iron Redox Control

Nitric Oxide–Triggered Remodeling of Chloroplast Bioenergetics and Thylakoid Proteins upon Nitrogen Starvation inChlamydomonas reinhardtii

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